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Fish - How to ask them the right questions
Abstract and Figures
Fish represent the largest radiation of vertebrates, with over 32,000 species known to date – more than all other vertebrate species combined. While fish possess many anatomical and perceptual adaptations to the aquatic environment, most experimental procedures used to study cognition in other species are readily adaptable to fish. Their small size, ease of handling and wide range of ecological niches have made fish a model species for cognitive research for well over a century.
It is impossible to do the vast literature any justice, so this chapter will focus predominantly on four model species: guppies (Poecilia reticulata), three-spined sticklebacks (Gasterosteus aculeatus) and goldfish (Carassius auratus), the most common species in cognitive research, and on zebrafish (Danio rerio), an important model organism in developmental biology and genetics that is gaining popularity in cognitive studies. In the first section of the chapter, we begin by giving an overview of some anatomical and perceptual traits of these species that are relevant to cognitive research. We then address some characteristics of their life cycle, ecology and social behavior that should be considered when studying cognition, and include some tricks for adapting cognitive tasks to this group. In the second section of the chapter, we briefly review the literature on each of the four species, giving some historical information on their use as a model species in cognition and behavior. In the last section of the chapter, we give practical examples and tips on husbandry and how to investigate spatial and social learning in fish, and how these tasks may be adapted to slightly different questions.
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... Finding an appropriate and adequate approach to the study of fish reproductive behaviour is a specific challenge [19,20]. Catarina Pouca and Culum Brown, for example, gave their paper a telling title: "Fishhow to ask them the right questions" [21]. Two important methodological issues relate to our study. ...
Non-random mating plays a key role in speciation and impacts the individual life history. Body size is known to be one of the most important traits on which the mate choice is based. Various patterns of body size preference are known in fish, but they have been studied in a limited number of species. Although the climbing perch (Anabas testudineus) is widespread and well known, a few reports of its spawning are published. Moreover, its breeding has only been described in captivity and in most cases it has been artificially induced with hormonal agents. This paper describes the main features of natural spawning of the climbing perch in aquarium compared to induced spawning. A positive size-assortative mating has been revealed. The mating system of Anabas has been shown to be flexible, presumably ranging from monogamy to polygamy. The results are discussed in the context of the general issue of the adequacy of fish behaviour research methods.
... Fish have become a standard taxon in animal cognition and behavioral ecology research Vila Pouca and Brown 2018a). Many vertebrate traits are highly conserved, including brain functions and neuronal pathways (Broglio et al. 2011;Rittschof et al. 2014), making fish suitable subjects in a range of subfields, including comparative cognition, behavioral genetics, and even neuropsychiatric research (Oliveira 2013;Stewart et al. 2014). ...
... Fish have become a standard taxon in animal cognition and behavioral ecology research Vila Pouca and Brown 2018a). Many vertebrate traits are highly conserved, including brain functions and neuronal pathways (Broglio et al. 2011;Rittschof et al. 2014), making fish suitable subjects in a range of subfields, including comparative cognition, behavioral genetics, and even neuropsychiatric research (Oliveira 2013;Stewart et al. 2014). ...
Methods for Fish Biology, 2nd edition
Chapter 16: Behavior
Julianna P. Kadar, Catarina Vila Pouca, Robert Perryman, Joni Pini-Fitzsimmons, Sherrie Chambers, Connor Gervais, and Culum Brown
doi: https://doi.org/10.47886/9781934874615.ch16
Kadar, J. P., C. V. Pouca, R. Perryman, J. Pini-Fitzsimmons, S. Chambers, C. Gervais, and C. Brown. 2022. Pages 593–642 in S. Midway, C. Hasler, and P. Chakrabarty, editors. Methods for fish biology, 2nd edition. American Fisheries Society, Bethesda, Maryland.
Humans interact with fish in a wide variety of contexts. Fish are rapidly becoming the go-to model for medical research because of the conservative nature of vertebrate physiology. We catch and grow fish in captivity for human consumption and frequently rear fish for release into the wild either to supplement wild populations to enhance fisheries or as a conservation measure. In all cases, understanding fish behavior is vital whether you are interested in stock management, conservation biology, or animal welfare (Brown 2015).
Gone are the days when fish were viewed as mindless automata. We now know that fish behavior is highly flexible, providing the plasticity to allow individuals to adjust to prevailing conditions or contexts (Bshary and Brown 2014). Their level of cognitive and behavioral sophistication is on par with the rest of the vertebrates (Bshary and Schäffer 2002; Vila Pouca and Brown 2018a; 2018b). Unsurprisingly, a change in behavior is often the first sign that something has shifted in the environment; thus, behavioral studies are at the forefront of environmental and ecotoxicological research (Brown 2012; Oulton et al. 2014). The massive diversity of fishes (currently more than 32,000 described species), and the range of niches they occupy, means that generalization is nearly impossible. Thankfully, the approaches for studying fish behavior are also many and varied and rapidly developing with changes in technology.
Here we provide a brief overview of some of the emerging methods for studying fish behavior. We will not be reviewing fish behavior in general since this is the topic of multiple books (e.g., Magnhagen et al. 2008; Brown et al. 2011), nor will we be providing a general overview of how to study animal behavior. Such details can readily be found in any of the many excellent texts on animal behavior or behavioral ecology (Davies 1991; Dugatkin and Earley 2004; Alcock 2005; Goodenough et al. 2009). Many people study fish behavior under captive conditions where it is possible to control the environment and observe behaviors that can be attributed to specific cognitive processes. In most instances, it is simply a matter of refining the standard methods to suit the aquatic environment and the species of interest. The main difficulties of studying fish behavior arise when trying to observe them in their natural environment. The underwater world is not a place with which most people are comfortable or familiar. Humans can stay only so long in the watery world of fishes, so many of the methods we describe here attempt to overcome these problems by studying fish behavior remotely.
The study introduced and evaluated learning paradigms for Maylandia callainos cichlids using a modified version of the rodent T-maze, filled with tank water (the "sunken" modification). Both male and female fish underwent training in two distinct conditioning paradigms. Firstly, simple operant conditioning involved placing a food reward in either the right or left compartment. Cichlids demonstrated the ability to purposefully find the bait within 6 days of training, with a persistent place preference lasting up to 6 days. Additionally, the learning dynamics varied with sex: female cichlids exhibited reduction in latency to visit the target compartment and consume the bait, along with a decrease in the number of errors 3 and 4 days earlier than males, respectively. Secondly, visually-cued operant conditioning was conducted, with a food reward exclusively placed in the yellow compartment, randomly positioned on the left or right side of the maze during each training session. Visual learning persisted for 10 days until reaction time improvement plateaued. Color preference disappeared after 4 consecutive check-ups, with no sex-related interference. For further validation of visually-cued operant conditioning paradigm, drugs MK-801 (dizocilpine) and caffeine, known to affect performance in learning tasks, were administered intraperitoneally. Chronic MK-801 (0.17 mg/kg) impaired maze learning, resulting in no color preference development. Conversely, caffeine administration enhanced test performance, increasing precision in fish. This developed paradigm offers a viable approach for studying learning and memory and presents an effective alternative to rodent-based drug screening tools, exhibiting good face and predictive validity.
With the increasingly global scale and scope of aquaculture, the need to match this development with improvements in fish welfare is a central societal and industry goal. We provide a comprehensive assessment of the farmed Atlantic salmon (Salmo salar) literature with targeted examples focusing on Atlantic salmon farmed in Tasmania, Australia. We synthesise insights from both small- and industry-scale perspectives, highlighting other reviews that provide discussions of particular sub-areas of farmed salmon research. We focus on recent advances and improved methods for farmed Atlantic salmon handling and management, behaviour, health issues and breeding. We also address wildlife interactions resulting from fish farming, as well as future research directions and system development. This review can serve as the basis for the development of aquaculture management guidelines that place individual fish welfare as a primary goal.
Fishes are complex animals, with emotions, individual personalities and intelligence. Humans have wide-ranging impacts on the lives and welfare of fishes, but until recently we have given very little thought to the suffering we cause. This is beginning to change as the gap between public understanding and the science on fish intelligence closes. Governments are increasingly recognising sentience in fishes, and other marine animals like octopuses and lobsters, and are reviewing animal welfare legislation to better include them. However, with trillions of fishes killed each for food, addressing welfare in fisheries and aquaculture is complex, and fisheries in particular have largely been left in the ‘too hard basket’. It doesn’t have to be this way. There are solutions—we can keep feeding our growing populations whilst also ensuring fishes are treated with respect and compassion. It’s a journey we need to start as soon as possible
With over 30,000 recognized species, fishes exhibit an extraordinary variety of morphological, behavioural, and life-history traits. The field of fish cognition has grown markedly with numerous studies on fish spatial navigation, numeracy, learning, decision-making, and even theory of mind. However, most cognitive research on fishes takes place in a highly controlled laboratory environment and it can therefore be difficult to determine whether findings generalize to the ecology of wild fishes. Here, we summarize four prominent research areas in fish cognition, highlighting some of the recent advances and key findings. Next, we survey the literature, targeting these four areas, and quantify the nearly ubiquitous use of captive-bred individuals and a heavy reliance on lab-based research. We then discuss common practices that occur prior to experimentation and within experiments that could hinder our ability to make more general conclusions about fish cognition, and suggest possible solutions. By complementing ecologically relevant laboratory-based studies with in situ cognitive tests, we will gain further inroads toward unraveling how fishes learn and make decisions about food, mates, and territories.
Scientists have built a significant body of research that shows that fishes display all the features
commonly associated with intelligence in mammals, and that they experience stress, fear and pain. These
findings have significant ramifications for animal welfare legislation, an area from which fishes have been
traditionally excluded. Our most detrimental interaction with fishes is through commercial fisheries and
aquaculture, an industry that feeds billions of humans and employs millions more. We have invented a
vast array of fishing methods that extract fishes from almost every region on the planet in an equally vast
range of violent and painful ways. Fisheries managers regularly fail to prevent overfishing to ensure
healthy populations of target species, have not adequately addressed the impacts on other marine
species and the broader environment, nor prevented human rights abuses on board fishing vessels. Fish
welfare has not been a consideration. Farmed fishes are under our control for their entire lives, and while
there are welfare guidelines available, where these are applied, the goal is primarily to maximise
production and reduce losses, rather than ensure good welfare. These industries are important to many of
us; however, we need to change these systems to address both welfare and sustainability. For fisheries
this means a reduction in the number of fishes killed, by addressing overfishing and wasteful capture
methods, and reducing the length of time fishes suffer during capture. For aquaculture this means
keeping fishes in more natural environments at lower densities, reducing transport and handling impacts,
and choosing species that cope better with farming. Both sectors need to develop humane slaughtering
practices. Fish behaviour and welfare experts will benefit from working with the people and systems that
are driving more ethical and sustainable practices in fisheries and farming, to help initiate improvements
that will benefit individual fishes and the broader marine environment, as well as the lives of those
working in the industry. We must ensure that where we do need to farm and capture fishes it is done
humanely, fairly and without unnecessary waste of trillions of lives. A simple way forward would be to
reduce our reliance on fish as a primary source of protein, particularly in wealthy countries where
alternatives abound.
People retrieve episodic memories about specific earlier events that happened to them. Accordingly, researchers have sought to evaluate the hypothesis that nonhumans retrieve episodic memories. The central hypothesis of an animal model of episodic memory is that, at the moment of a memory assessment, the animal retrieves a memory of the specific earlier event. Testing this hypothesis requires the elimination of nonepisodic memory hypotheses. A number of case studies focus on the development of animal models of episodic memory, including what-where-when memory, source memory, item-in-context memory, and unexpected questions. Compelling evidence for episodic memory comes from studies in which judgments of familiarity cannot produce accurate choices in memory assessments. These approaches may be used to explore the evolution of cognition.
The ability to respond flexibly to environmental challenges, for instance by learning or by responding appropriately to novel stimuli, may be crucial for survival and reproductive success. Experiences made during early ontogeny can shape the degree of behavioural flexibility maintained by individuals during later life. In natural habitats, animals are exposed to a multitude of social and non-social ecological factors during early ontogeny, but their relative influences on future learning ability and behavioural flexibility are only poorly understood. In the cooperatively breeding cichlid Neolamprologus pulcher, we investigated whether early social and predator experiences shape the learning performance, flexibility, and response to novelty of adults. Fish were reared either with or without parents and helpers and with or without perceived predation risk in a full-factorial experiment. We investigated the influence of these treatments on learning performance and flexibility in a spatial acquisition and reversal learning task. To test for response to novelty, we performed a neophobia test. We found that fish reared with predator experience, but without the presence of older group members outperformed fish with other rearing backgrounds in reversal learning and that individuals, which had been reared in a socially more complex environment together with older group members responded less neophobic toward a novel object than individuals reared among siblings only. Comparative evidence from fish and rats suggests that these developmental effects may be driven by the cues of safety perceived in the presence of guarding parents.
The communication of aggressive propensity is an important component of agonistic interactions. For this purpose, animals use different sensory modalities involving visual, acoustical and chemical cues. While visual and acoustic communication used in aggressive encounters has been studied extensively in
a wide range of taxa, the role of chemical communication received less attention. Here, we studied the role of chemical cues used during agonistic interactions of territory owners in the cooperative cichlid Neolamprologus pulcher. During staged encounters, we allowed either visual and chemical contact
between two contestants or visual contact only. As chemical information in this species is most likely transferred via urine, we measured urination patterns using dye injections. Furthermore, we recorded aggressive and submissive behaviours of both contestants in response to the experimental treatment. Fish that had only visual contact with each other significantly increased their urination frequency and showed more aggressive displays compared to fish with both visual and chemical contact. Furthermore, appropriate agonistic responses appear to be dependent on available chemical information. This indicates that N. pulcher actively emits chemical signals to communicate their aggressive propensity via urine.
Chemical communication thus plays a crucial role in multimodal communication of aggression in these fish, which highlights the need of studying the role of chemical communication during agonistic encounters in general, even if other signals are more obvious to the human observer.
Significance
Within social groups, there are animals of different social status that express different behavioral profiles that are paralleled by different patterns of gene expression in the brain. However, social status is not fixed, but rather depends on social interactions; hence, group living animals must be able to switch between different status-dependent behavior and brain gene expression profiles. Here we show for the first time, to our knowledge, that what triggers a genomic response to a social interaction in zebrafish is the subjects’ assessment of the interaction rather than a fixed response to a releaser cue in the environment. The occurrence of fighting assessment in zebrafish suggests that a cognitive ability classically considered complex is also present in a simple-minded vertebrate.
Public information is widely available at low cost to animals living in social groups. For instance, bystanders may eavesdrop on signaling interactions between conspecifics and use it to adapt their subsequent behavior towards the observed individuals. This social eavesdropping ability is expected to require specialized mechanisms such as social attention, which selects social information available for learning. To begin exploring the genetic basis of social eavesdropping, we used a previously established attention paradigm in the lab to study the brain gene expression profile of male zebrafish (Danio rerio) in relation to the attention they paid towards conspecifics involved or not involved in agonistic interactions. Microarray gene chips were used to characterize their brain transcriptomes based on differential expression of single genes and gene sets. These analyses were complemented by promoter region-based techniques. Using data from both approaches, we further drafted protein interaction networks. Our results suggest that attentiveness towards conspecifics, whether interacting or not, activates pathways linked to neuronal plasticity and memory formation. The network analyses suggested that fos and jun are key players on this response, and that npas4a, nr4a1 and egr4 may also play an important role. Furthermore, specifically observing fighting interactions further triggered pathways associated to a change in the alertness status (dnajb5) and to other genes related to memory formation (btg2, npas4b), which suggests that the acquisition of eavesdropped information about social relationships activates specific processes on top of those already activated just by observing conspecifics.
Group living animals may eavesdrop on signalling interactions between conspecifics in order to collect adaptively relevant information obtained from others, without incurring in the costs of first-hand information acquisition. This ability (aka social eavesdropping) is expected to impact Darwinian fitness, and hence predicts the evolution of cognitive processes that enable social animals to use public information available in the environment. These adaptive specializations in cognition may have evolved both at the level of learning and memory mechanisms, and at the level of input mechanisms, such as attention, which select the information that is available for learning. Here we used zebrafish to test if attention in a social species is tuned to the exchange of information between conspecifics. Our results show that zebrafish are more attentive towards interacting (i.e. fighting) than towards non-interacting pairs of conspecifics, with the exposure to fighting not increasing activity or stress levels. Moreover, using video playbacks to manipulate form features of the fighting fish, we show that during the assessment phase of the fight, bystanders' attention is more driven by form features of the interacting opponents; whereas during the post-resolution phase, it is driven by biological movement features of the dominant fish chasing the subordinate fish.
Identification of individuals is a prerequisite in many behavioural studies. Visible Implant Elas-tomer (VIE) colour tags are a well-established way to mark animals. VIE tagging does not seem to affect individual growth or survival. However, studies verifying their neutrality during social interactions are less common. Here, individual male and female zebrafish Danio rerio were simultaneously given the choice between two shoals, each consisting of six fish. Members of one shoal were uniformly marked with one VIE tag of a given colour, whereas the other shoal was sham-tagged. In total, 10 different colours were used. Test fish spent significantly more time near the tagged shoal (56%) than near the sham-tagged shoal (44%). Tag colour did not significantly influence the preferences. The results highlight the importance of confirming the neutrality of colour tags before using them in behavioural studies. Especially, our study advises caution when using marked and unmarked fish simultaneously.
The behaviour of animals towards their mirror image (“mirror test”) is routinely used as a proxy to measure aggression levels, especially in fish. The lack of evidence for visual self-recognition in fish supports this method. However, recent work points towards different hormonal and gene expression responses when fish are exposed either to conspecific opponents or to their mirror image, urging for validation of this widespread method. Here, we test the predictive value of mirror tests in three sympatric cichlid species from Lake Tanganyika: the cooperative breeder Neolamprologus pulcher, the polygamous shell brooder Telmatochromis vittatus and the monogamous, biparental piscivore Lepidiolamprologus elongatus. In particular, we compare differences in restrained and overt aggression levels for individuals of each species when confronted with a mirror or a live conspecific. The three species differed in response to the two contest situations. While in N. pulcher both aggressive responses were correlated between the mirror test and the live opponent fight, there was no such relationship in T. vittatus and L. elongatus. Thus, the mirror test appears to be a suitable surrogate for intraspecific aggression in N. pulcher, while aggression against a mirror image has limited predictive value for intraspecific aggression in the other two species. These results underline the importance of validating the mirror test’s predictive value in a study species before drawing conclusions from mirror tests about aggressiveness under natural, social conditions.
Motion illusion refers to a perception of motion that is absent or different in the physical stimulus. These illusions are a powerful non-invasive tool for understanding the neurobiology of vision because they tell us, indirectly, how we process motion. There is general agreement in ascribing motion illusion to higher-level processing in the visual cortex, but debate remains about the exact role of eye movements and cortical networks in triggering it. Surprisingly, there have been no studies investigating global illusory motion evoked by static patterns in animal species other than humans. Herein, we show that fish perceive one of the most studied motion illusions, the Rotating Snakes. Fish responded similarly to real and illusory motion. The demonstration that complex global illusory motion is not restricted to humans and can be found even in species that do not have a cortex paves the way to develop animal models to study the neurobiological bases of motion perception.
Variation in the structural complexity of a habitat is known to have significant affects on the evolution of different populations
and can shape behavior, morphology, and life-history traits. Here, we investigated whether habitat complexity influences a
species’ capacity for spatial learning and cue choice by comparing the performance of 4 goby species from 2 contrasting habitats
in a spatial task. Gobies were collected from dynamic, homogenous sandy shores and stable, spatially complex rock pool habitats.
We trained fish to use a T-maze to find a hidden reward and asked whether they used local visual landmarks or body-centered
methods for orientation (i.e. turn direction) to do so. It was expected that fish from rock pools would learn the spatial
task much faster and use different orientation cues than fish from sandy shores. We found that rock pool species learnt the
location of the reward arm much faster, made fewer errors and used both types of cues available (visual landmarks and turn
direction) to locate the reward, whereas sand species relied on turn direction significantly more than plant landmarks to
orientate. The results of this study provide support for the hypothesis that the spatial complexity of habitats in marine
environments has a significant effect on the evolution of fish cognition.
Recent studies on animal mathematical abilities suggest that all vertebrates show comparable abilities when they are given spontaneous preference tests, such as selecting the larger number of food items, but that mammals and birds generally achieve much better performance than fish when tested with training procedures. At least part of these differences might be due to the fact that fish are usually trained with only one or two dozen trials while extensive training, sometimes with thousands of trials, is normally performed in studies of mammals and birds. To test this hypothesis, female guppies were trained on four consecutive numerical discriminations of increasing difficulty (from 2 vs. 3 to 5 vs. 6 items), with up to 120 trials with each discrimination. Five out of eight subjects discriminated all contrasts up to 4 vs. 5 objects at levels significantly better than chance, a much higher limit than the 2 vs. 3 limit previously reported in studies that provided fish with only short training sequences. Our findings indicate that the difference in numerical cognition between teleosts and warm blooded vertebrates might be smaller than previously supposed.
One of the main challenges in the study of social networks in vertebrates is to close the gap between group patterns and dynamics. Usually scan samples or transect data are recorded to provide information about social patterns of animals, but these techniques themselves do not shed much light on the underlying dynamics of such groups. Here we show an approach which captures the fission-fusion dynamics of a fish population in the wild and demonstrates how the gap between pattern and dynamics may be closed. Our analysis revealed that guppies have complex association patterns that are characterised by close strong connections between individuals of similar behavioural type. Intriguingly, the preference for particular social partners is not expressed in the length of associations but in their frequency. Finally, we show that the observed association preferences could have important consequences for transmission processes in animal social networks, thus moving the emphasis of network research from descriptive mechanistic studies to functional and predictive ones.
It has been known for more than a century that interacting people can generally achieve more accurate decisions than single individuals. Here we show that interacting guppy fish (Poecilia reticulata) achieve a superior level of numerosity discrimination well beyond the average ability of the isolated individual fish. This enhancement of numerical acuity was observed in dyadic interactions when (Experiment 1) the dyad chose which larger shoal of guppies to join and when (Experiment 2) the dyad chose the higher or the lower numerosity among two decision options after having learned the task individually. Dyadic accuracy and that of the more competent member of each dyad matched closely, supporting the hypothesis that meritocratic leadership arises spontaneously between dyadically interacting fish, rather than the 'many wrongs' principle that has been used to explain group superiority in many species.
The acquisition of information such as the location and quality of food, mates or shelter is a key survival
requirement for animals. Individuals can acquire information through personal experience (private information)
or through observing and interacting with others (social information). Environmental spatial
and temporal heterogeneity can mean that sometimes social information conflicts with private knowledge.
We tested how personality affected the importance placed on public versus private information in
wild female guppies when these two information sources came into conflict.We found that boldness and
sociality affected decisions to use conflicting social and private information. Bolder females used social
information to avoid competition and/or potential patch depletion, whereas highly social individuals
preferred the presence of conspecifics over rich foraging opportunities. There was no evidence of a speed
eaccuracy trade-off in a spatial associative learning task; rather, bold female guppies learned both more
quickly and more accurately than shy females. We found no evidence of a behavioural syndrome between
boldness and sociality which is consistent with previous studies on this population.
Figure 1. Feeding propensity of female guppies selected for large and small brain size when offered a novel food source (a pellet instead of flake food: 0 = never, 1 = always). Food was given once per day for 7 consecutive days. Feeding propensity is the number of times the fish ate the pellet (out of seven times). To analyse feeding propensity we used a binary general linear mixed model with feeding (yes/no) as the dependent variable, brain size treatment as a fixed factor, and replicate line, day of feeding and individual as random factors (GLMM: F = 1.945, N = 24, P = 0.176; the figure shows the mean estimated marginal means ± SE of this GLM).
Social competence is defined as the ability of an animal to optimize the expression of social behaviour as a function of the available social information. The social environment encountered early in life can affect the expression of various social behaviours later in life. We investigated whether early social experience can affect social competence. In the cooperatively breeding cichlid Neolamprologus pulcher, we tested whether individuals reared with older brood-caring conspecifics persistently perform better in a series of tasks (1) simulating different social contexts, (2) assigning individuals different social roles and (3) exposing them to an unknown social situation. Fish that had been reared together with older conspecifics showed more appropriate behaviours both as winners (more aggressive displays) and as losers (more submissive displays) when aggressively competing with peers over a resource, and when trying to be accepted as subordinate group member and prospective brood care helper by an unfamiliar dominant pair (more submissive displays near shelters), a situation they had never encountered before. In both tasks fish that had grown up with older fish were tolerated better by conspecifics than fish reared with same-age siblings only. We detected effects of the early environment on social behaviour in the juvenile and adult stages of the test fish. Our results suggest that growing up in more complex social groups fosters a general social ability (i.e. social competence) in N. pulcher that improves their performance across different social roles and contexts, and which may provide fitness benefits.
It has been widely recognized that size, shape, and distance perception are not the mere translation of images in the eyes, as retinal images are inherently ambiguous. Some form of knowledge and/or assumptions by unconscious inductive inference seems to be necessary (Gregory, 1997). With respect to this topic, visual illusions are a valuable tool for understanding the neuro-cognitive systems underlying visual perception by indirectly revealing the hidden constraints of the perceptual system in a way that normal perception cannot. In humans, such constraints have been often summarized as the so-called “Gestalt principles,” which can be briefly described by the motto “the whole is greater than the sum of its parts” (Wertheimer, 1938). Almost a century of experimental investigation on visual illusions has broadened our comprehension of the perceptual mechanisms that enable us to perceive figures and forms instead of just a collection of lines and curves. Such mechanisms are highly adaptive, as they allow for a quick and stable picture of the environment, enabling an appropriate motor response in every context (Ikin and Turner, 1972).
There is controversy in comparative psychology about whether on the one hand non-symbolic number estimation of small (≤4) and large numbers involves a single mechanism (an approximate number system), or whether on the other hand enumeration of the numbers 1-4 is accomplished by a separate mechanism, an object tracking system. To date, support for the latter hypothesis has come only from the different ratio-dependency of performance seen in the two numerical ranges, a reading that has been criticized on several grounds. In humans, the two-system hypothesis is supported by evidence showing that manipulation of the physical properties of the stimuli (e.g., the motion of the items) has dissimilar effects on small- and large-number discrimination. In this research, we studied this effect on guppies. Initially, fish were trained to simultaneously discriminate two numerical contrasts having the same easy ratio (0.50): one in the small-number (2 vs. 4) range and one in the large-number (6 vs. 12) range. Half of the fish were presented with moving items; the other half were shown the same stimuli without motion. Fish were then subjected to non-reinforced probe trials in the presence of a more difficult ratio (0.75: 3 vs. 4 and 9 vs. 12). Under both static and moving conditions, the fish significantly discriminated 6 versus 12, but not 9 versus 12 items. As regards small numbers, both groups learned to discriminate a 0.50 ratio, but only fish tested with moving stimuli also discriminated 3 and 4 items. This differential effect suggests that fish may possess two separate systems for small- and large-number discrimination.
In this study, pairs of juvenile sticklebacks either familiar with each other or pairs
unfamiliar with each other met to share a food source. The study showed that
sticklebacks were less aggressive towards a partner when sharinga common food
source with a familiar conspecific, compared to when sharing a food source with an
unfamiliar conspecific. The results showedt hat the aggressive behaviour was built up
and broken down gradually depending on how long the two competitors had been
together or apart. A decreasei n aggressivenes was found after the sticklebacks had
been together two weeks, with a further decrease after four weeks together. Conversely
there was an increase in aggressivenes after the sticklebacksh ad been parted
for two weeks or four weeks. The chance of food being equally distributed between
the competing pairs increased with time spent together and decreased with time
parted.The observed decrease or increase in the amount of aggression is discussed as
a build-up or a breakdown of rank knowledge or of a co-operative partnership
Adult social behaviour can be persistently modified by early-life social experience. In rodents, such effects are induced by tactile maternal stimulation resulting in neuroendocrine modifications of the hypothalamic-pituitary-adrenal axis involved in stress responsiveness. Whether similar long-term alterations can occur in the hypothalamic-pituitary-interrenal (HPI) axis of poikilothermic vertebrates is unknown. We compared the expression of four genes of the HPI axis in adults of the cooperatively breeding cichlid Neolamprologus pulcher, which had been exposed to two early-life social treatments 1.5 years prior to brain sampling. Fish reared with parents and siblings had less brain expression of corticotropin-releasing factor and of the functional homologue of the mammalian glucocorticoid receptor (GR1) than individuals reared with same-age siblings only. Expression of the mineralocorticoid receptors (MR) did not differ between treatments, but the MR/GR1 expression ratio was markedly higher in fish reared with parents and siblings. Thus, we show here that early social experience can alter the programming of the stress axis in poikilothermic vertebrates, suggesting that this mechanism is deeply conserved within vertebrates. Moreover, we show for the first time that reprogramming of the stress axis of a vertebrate can be induced without tactile stimulation by parents.
In the underwater environment, sound propagates as both a pressure wave and as particle displacement, with particle displacement dominating close to the source (the nearfield). At the receptor level, both the fish ear and the neuromast hair cells act as displacement detectors and both are potentially stimulated by the particle motion component of sound sources, especially in the nearfield. A now common way to test 'hearing' in fish involves auditory evoked potentials (AEP), with recordings made from electrodes implanted near the auditory brainstem. These AEP recordings are typically conducted in enclosed acoustic environments with the fish well within the nearfield, especially for lower frequencies. We tested the contribution of neuromast hair cells to AEP by first testing intact goldfish (Carassius auratus), then ablating their neuromasts with streptomycin sulfate - disabling superficial and canal neuromasts - and retesting the same goldfish. We did a similar experiment where only the superficial neuromasts were physically ablated. At 100 and 200 Hz, there was a 10-15 dB increase in threshold after streptomycin treatment but no significant difference at higher frequencies. There was no difference in threshold in control fish or in fish that only had superficial neuromasts removed, indicating that the differential responses were driven by canal neuromasts. Taken together these results indicate that AEP results at lower frequencies should be interpreted as multimodal responses, rather than 'hearing'. The results also suggest that in natural situations both the ear and lateral line likely play an integrative role in detecting and localising many types of 'acoustic' stimuli.
Darwin famously described special difficulties in explaining social evolution in insects. More than a century later, the evolution of sociality - defined broadly as cooperative group living - remains one of the most intriguing problems in biology. Providing a unique perspective on the study of social evolution, this volume synthesizes the features of animal social life across the principle taxonomic groups in which sociality has evolved. The chapters explore sociality in a range of species, from ants to primates, highlighting key natural and life history data and providing a comparative view across animal societies. In establishing a single framework for a common, trait-based approach towards social synthesis, this volume will enable graduate students and investigators new to the field to systematically compare taxonomic groups and reinvigorate comparative approaches to studying animal social evolution.
Keywords: fish behaviour mirror test Poecilia reticulata shoaling sociability Many fish species are social, and individuals spend most of their lives in shoals, but sociability can vary greatly between species, populations and individuals. Sociability has been largely studied by measuring the time spent by a focal fish in proximity to one or more conspecifics. To control for the behaviour of the stimulus fish, the conspecifics have often been substituted by a mirror, on the assumption that the subject perceives its mirror image as a conspecific. The validity of the mirror test has recently been questioned, at both the behavioural and the molecular level, because of the discrepancy in fish responses when exposed to a mirror image and to a live conspecific. In this study, we compared the sociability scores of a social fish, the guppy, Poecilia reticulata, obtained using live fish or a mirror as a stimulus, to assess the validity of the mirror test. We found that the sociability score assessed using the standard mirror test was not significantly correlated with the sociability assessed using live stimuli. Nevertheless, we observed a positive correlation between the scores of the two tests when the mirror test was performed in a more naturalistic context, controlling for the minimum distance between the stimulus fish and the mirror. Our findings provide evidence of the reliability of the mirror test as a measure of so-ciability compared to the test using live conspecifics when certain requirements are satisfied.
The early social environment can have substantial, lifelong effects on vertebrate social behaviour, which can be mediated by developmental plasticity of brain gene expression. Early life effects can influence immediate behavioural responses towards later-life social challenges and can activate different gene expression responses. However, while genomic responses to social challenges have been reported frequently, how developmental experience influences the shape of these genomic reaction norms remains largely unexplored. We tested how manipulating the early social environment of juvenile, cooperatively-breeding cichlids, Neolamprologus pulcher, affects their behavioural and brain genomic responses when competing over a resource. Juveniles were reared either with or without a breeder pair and a helper. Fish reared with family members behaved more appropriately in the competition than when reared without. We investigated whether the different social rearing environments also affected the genomic responses to the social challenge. A set of candidate genes, coding for hormones and receptors influencing social behaviour, were measured in the telencephalon and hypothalamus. Social environment and social challenge both influenced gene expression of egr-1 (early growth response 1) and gr1 (glucocorticoid receptor 1) in the telencephalon and of bdnf (brain derived neurotrophic factor) in the hypothalamus. A global analysis of the 11 expression patterns in the two brain areas showed that neurogenomic states diverged more strongly between intruder fish and control fish when they had been reared in a natural social setting. Our results show that same molecular pathways may be used differently in response to a social challenge depending on early life experiences. This article is protected by copyright. All rights reserved.
The performance of goldfish was examined under two-component chained and tandem food reinforcement schedules with and without brief stimuli added. Both food-paired and nonpaired brief stimuli were evaluated under conditions in which each component schedule was a fixed-interval 90- sec and the operant response was contact with the feeder tube. In general, the chained schedule engendered a higher rate of responding than the tandem schedule. Responding within a schedule occurred at the highest rate when a food-paired brief stimulus (tone) was used. The brief stimulus not paired with food had little effect on responding. Under both the tandem and chained schedules, a pronounced pattern of positively accelerated responding was observed within the initial component when the food-paired brief stimulus was presented. These results indicate that in goldfish, as in better studied species, a briefly presented food-paired stimulus is a more effective conditioned reinforcer than the presentation of a discriminative stimulus associated with a schedule component under which food is earned, which is in turn more effective than a nonpaired brief stimulus.
The effect of visible implant elastomer (VIE) tagging on the immediate physiological stress response was tested in female three-spined stickleback Gasterosteus aculeatus, using non-invasive waterborne cortisol analysis. Post-tagging cortisol levels were significantly higher compared with pretreatment baseline concentrations; however, when comparing post-tagging cortisol levels with cortisol levels after exposure to a simulated aerial predator, no significant differences were found. This study indicates that VIE tagging elicits a physiological stress response similar to those occurring in the everyday lives of this important biological model organism.
© 2015 The Fisheries Society of the British Isles.
There is a well-established tradition of studying numerical abilities in mammals and birds; however, only recently has it been proposed that some species of fish possess similar capacities. Here we review the evidence for the presence of rudimentary numerical abilities in fish. There is substantial evidence that fish can use purely numerical information both when they are trained to discriminate among different quantities and when they are required to choose which group of social companions is less/more numerous. In both contexts, however, they tend to use primarily continuous quantities (e.g., area) instead of discrete numbers when both types of information are available. Similarities among species appear greater than differences and, in general, fish numerical capacities closely match those reported in mammals and birds. The study of developmental trajectories suggests that fish have multiple core number systems that are domain-specific and serve to solve a limited set of problems.
This paper describes and evaluates a flexible, non-invasive tagging system for the automated identification and long-term monitoring of individual three-spined sticklebacks Gasterosteus aculeatus. The system is based on barcoded tags, which can be reliably and robustly detected and decoded to provide information on an individual's identity and location. Because large numbers of fish can be individually tagged, it can be used to monitor individual- and group-level dynamics within fish shoals.
Abstract The zebrafish offers an excellent compromise between system complexity and practical simplicity and has been suggested as a translational research tool for the analysis of human brain disorders associated with abnormalities of social behavior. Unlike laboratory rodents zebrafish are diurnal, thus visual cues may be easily utilized in the analysis of their behavior and brain function. Visual cues, including the sight of conspecifics, have been employed to induce social behavior in zebrafish. However, the method of presentation of these cues and the question of whether computer animated images versus live stimulus fish have differential effects have not been systematically analyzed. Here, we compare the effects of five stimulus presentation types: live conspecifics in the experimental tank or outside the tank, playback of video-recorded live conspecifics, computer animated images of conspecifics presented by two software applications, the previously employed General Fish Animator, and a new application Zebrafish Presenter. We report that all stimuli were equally effective and induced a robust social response (shoaling) manifesting as reduced distance between stimulus and experimental fish. We conclude that presentation of live stimulus fish, or 3D images, is not required and 2D computer animated images are sufficient to induce robust and consistent social behavioral responses in zebrafish.
Migratory marine animals exploit resources in different oceanic regions at different life stages, but how they navigate to specific oceanic areas is poorly understood [1-3]. A particular challenge is explaining how juvenile animals with no prior migratory experience are able to locate specific oceanic feeding habitats that are hundreds or thousands of kilometers from their natal sites [1-7]. Although adults reproducing in the vicinity of favorable ocean currents can facilitate transport of their offspring to these habitats [7-9], variation in ocean circulation makes passive transport unreliable, and young animals probably take an active role in controlling their migratory trajectories [10-13]. Here we experimentally demonstrate that juvenile Chinook salmon (Oncorhynchus tshawytscha) respond to magnetic fields like those at the latitudinal extremes of their ocean range by orienting in directions that would, in each case, lead toward their marine feeding grounds. We further show that fish use the combination of magnetic intensity and inclination angle to assess their geographic location. The "magnetic map" of salmon appears to be inherited, as the fish had no prior migratory experience. These results, paired with findings in sea turtles [12-21], imply that magnetic maps are phylogenetically widespread and likely explain the extraordinary navigational abilities evident in many long-distance underwater migrants.
One-way mirrors were used to determine whether male three-spined sticklebacks, Gasterosteus aculeatus, could use visual cues to distinguish between pairs of neighbours that had similar social and physical attributes. Neighbours were enclosed in identical tanks that had no physical landmarks. The tanks had opaque side-walls and one-way mirrors (reflecting inward) placed along end-walls; thus, neighbours could not see outside of their tanks. Neighbour tanks were positioned at the ends of a test tank so that a resident could view both neighbours. Tanks were left undisturbed until residents completed a nest (ca 4-6 days). If neighbours were then switched from one end of a residents' territory to the other, residents charged toward and bit at the neighbours more often than they did following a 'mock' switch (i.e. neighbours were moved but then returned to their original position); following actual switches, males also devoted less effort to nest maintenance. Furthermore, the amount of effort devoted to defending a given side of the tank depended on which neighbour was there. The neighbours' surroundings did not change after switches, nor did their behaviour. Thus, male sticklebacks can distinguish between familiar rivals using visual cues alone. The ability developed in 4-6 days (i.e. the time required to build nests) and did not require physical interaction with the neighbours.
The view that the human mind is a repository of stored items dates at least to Aristotle and Plato and continues to dominate investigations of human memory [1]. This view fits with our intuitions that we study information as the optimal method to store information in memory and that retrieval of information functions only to assess what information was previously stored. Yet modern research on human memory suggests that retrieving information during a test facilitates later memory of that information [2-6]. Because human memory is intertwined with language, it is difficult to resist the conclusion that language is essential for this key aspect of human cognition. Here we show that practising memory retrieval improves long-term retention in a nonhuman species. We report evidence that rats' long-term memory performance is enhanced if they had previously retrieved specific items stored in memory.
Laboratory-reared predator-naive three-spined sticklebacks from two sites, one with abundant predatory fish (the high-risk site) and the other essentially predator-free (the low-risk site), were given a passive avoidance conditioning task in which they received a simulated attack from a model avian predator whenever they entered a previously-favoured feeding patch. 15/16 fish learned to avoid the dangerous patch within 15 days, but those from the high-risk site did so significantly faster and received fewer attacks in the process. The two categories of fish did not differ either in active avoidance of the attack stimulus or in the rate at which they started to re-exploit the dangerous patch once negative reinforcement ceased. It is argued that fish from high- and low-risk sites differ in the negatively reinforcing properties of the same, standardised attack.
Goldfish, Carassius auratus, were introduced into an arena tank containing two symmetrically placed gravel-filled trays, one of which contained hidden food. In the absence of additional structures in the tank, the accuracy of food-patch choice (i.e. the proportion of individuals contacting the full tray before the empty tray) was close to that expected assuming random binary choice. Accuracy improved significantly, however, when landmarks (a rock/plant combination or multicoloured plastic columns) were positioned close to the food patch. Choice performance also improved when the plastic columns were placed in the opposite (non-food) half of the tank, indicating a capacity for indirect landmark usage as distinct from direct visual cueing. Latencies to feeding decreased with experience in all tratments, but were significantly lower in the presence of landmarks. Exploratory sampling behaviour, as indicated by the number of visits to the empty patch once food had been found during a trial, was significantly less frequent in the presence of strong landmarks. Fish in all treatments increased the frequency of sampling visits following a reversal of full and empty patches. Reliance on memory-based spatial behaviour may therefore vary according to the nature and complexity of the visual environment.
To forage efficiently in a patchy environment animals must make informed decisions concerning in which patches to forage, for which the behaviour of other animals often provides informative cues. However, other individuals may differ in the quality or relevance of information that they provide, and accordingly animals are expected to be selective with respect to whom they copy. Such selectivity may include the biasing of copying towards older, larger or more experienced conspecifics. We investigated whether the ability of nine-spined sticklebacks, Pungitius pungitius, to exploit public information, that is, to judge the relative profitability of food patches solely on the basis of the relative feeding activity of others, is influenced by their own body size and that of the individuals from whom they copy. Individual observer fish, classed as either small or large, were trained that two discrete foraging patches differed in their relative quality, one being rich and the other poor ('personal information'). They then watched two shoals of either small or large demonstrator conspecifics feeding at the two patches ('public informa- tion'), but with relative profitability of the patches reversed compared to training, before being given the opportunity to make a patch choice. The effectiveness of this public demonstration was clearly contin- gent on the size of the demonstrators, with subjects of both size classes copying the patch choice of large demonstrators significantly more than they copied the patch choice of small demonstrators. This study reinforces the view that animal social learning is directed along particular pathways, with individuals predisposed by selection to copy particular categories of individual differentially.
Shoaling fish are expected, in many cases, to gain fitness benefits from being in a larger shoal and previous experiments have shown that fish are indeed capable of choosing between shoals of different sizes. We investigated the influence of shoal activity on shoal size preference in the zebrafish. We gave test fish the choice between shoals of one to four stimulus fish, presented at two different water temperatures, and so differing in their activity levels. Where all stimulus fish were in water of the same temperature, test fish generally preferred the larger shoal. However, this preference could be reduced by presenting the larger shoal in colder water and so reducing its activity. We discuss these findings with reference to the factors that may influence shoal activity, the effect of temperature on shoaling behaviour and the mechanisms that may be used by fish to discriminate shoal size.
In the "standard-opponent' test the test subject fights against a much smaller opponent behind a transparent partition, whereas in the mirror test it attacks its own mirror image. When fish had been involved in a series of escalating activities without final decision of the encounters, in subsequent mirror tests their biting frequencies were elevated for at least 24h after the last fight. Winning a rank order fight led to an increase and losing to a decrease in biting frequency 24h later. After social settlement in a long-term stabilized social hierarchy the relation is totally reversed: dominant males showed much lower biting frequencies than subordinate males in the mirror test. The hypothesis is proposed that even under natural conditions high ranking males tend to use their energy potential in a more economic way than low ranking males. The existence of rank-dependent fighting strategies could be due to differences in risk: the fighting activities of dominant males are extremely risky because they can lose their high social status, which inevitably would lead to a lowered genetic fitness, whereas the aggressive actions of subordinate males are not very risky because their social status is low anyway. -from Authors
Source memory is a representation of the origin (source) of information. When source information is bound together, it makes a memory episodic, allowing us to differentiate one event from another [1
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]. Here, we asked whether rats remember the source of encoded information. Rats foraged for distinctive flavors of food that replenished (or failed to replenish) at its recently encountered location according to a source-information rule. To predict replenishment, rats needed to remember where they had encountered a preferred food type (chocolate) with self-generated (walking along a runway encountering chocolate) or experimenter-generated (placement of the rat at the chocolate site by an experimenter) cues. Three lines of evidence implicate the presence of source memory. First, rats selectively adjusted revisits to the chocolate location based on source information, under conditions in which familiarity of events could not produce successful performance. Second, source memory was dissociated from location memory by different decay rates. Third, temporary inactivation of the CA3 region of the hippocampus with lidocaine selectively eliminated source memory, suggesting that source memory is dependent upon an intact hippocampus. Development of an animal model of source memory may be valuable to probe the biological underpinnings of memory disorders marked by impairments in source memory.
Previous studies have shown that guppies, Poecilia reticulata, can learn the route to a food source by shoaling with knowledgeable conspecifics, and prefer to shoal with experienced foragers and familiar fish. We tested the hypothesis that guppies would learn more effectively from (1) familiar than unfamiliar demonstrators and (2) well-trained than poorly trained demonstrators. Demonstrator fish were given experience in swimming a route to a food source and then introduced into shoals of untrained observer guppies; the spread of this foraging skill was recorded over 15 trials. The demonstrators were either familiar or unfamiliar to the observers and either well trained or poorly trained. Observers performed significantly better when the demonstrators were familiar. The training of the demonstrators made no overall difference to the performance of naıve observers. However, whilst observers in shoals exposed to well-trained demonstrators did better initially than those with poorly trained ones, the latter learned the route to the feeder faster. Our results suggest that familiarity may generate a form of directed social learning in guppy shoals, in which fish learn more effectively from familiar conspecifics. An analysis of who follows whom suggests that well-trained demonstrators can provide a ‘tip-off’ as to the location of the hole but poorly trained demonstrators were more likely to be followed. The results suggest that while observers are able to shoal with poorly trained demonstrators, well-trained demonstrators swim the maze route too quickly to be followed, but may attract attention to the maze route.